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Sensory detection of female olfactory cues as a central regulator of energy metabolism and body weight in male mice.

ABSTRACT: Olfactory stimuli from food influence energy balance, preparing the body for digestion when food is consumed. Social chemosensory cues predict subsequent energetic changes required for social interactions and could be an additional sensory input influencing energy balance. We show that exposure to female chemostimuli increases metabolic rate in male mice and reduces body weight and adipose tissue expansion when mice are fed a high-fat diet. These responses are linked to detection of female chemostimuli via G-protein Gαo-expressing vomeronasal sensory neurons. Males with Gαo deleted in the olfactory system are fertile but do not show changes in body weight when paired with females and show severely blunted changes in energy expenditure when exposed to female bedding. These results establish that metabolic and reproductive responses to females can be partly uncoupled in male mice and that detection of female chemostimuli is a central regulator of energy metabolism and lipid storage.

SUBMITTER: Garratt M

PROVIDER: S-EPMC10067763 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Sensory detection of female olfactory cues as a central regulator of energy metabolism and body weight in male mice.

Garratt Michael M Neyt Christine C Ladyman Sharon R SR Pyrski Martina M Zufall Frank F Leinders-Zufall Trese T

iScience 20230320 4

Olfactory stimuli from food influence energy balance, preparing the body for digestion when food is consumed. Social chemosensory cues predict subsequent energetic changes required for social interactions and could be an additional sensory input influencing energy balance. We show that exposure to female chemostimuli increases metabolic rate in male mice and reduces body weight and adipose tissue expansion when mice are fed a high-fat diet. These responses are linked to detection of female chemo ...[more]

PMID: 37020965

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Project description:The maternal environment has been shown to influence female olfactory preferences through early chemosensory experience. However, little is known about the influence of the maternal environment on chemosignals. In this study, we used two inbred mouse strains, C57BL/6 (C57) and BALB/c (BALB), and explored whether adoption could alter male chemosignals and thus influence female olfactory preferences. In Experiment 1, C57 pups were placed with BALB dams. Adult BALB females then served as the subjects in binary choice tests between paired male urine odours (BALB vs. C57, BALB vs. adopted C57 and C57 vs. adopted C57). In Experiment 2, BALB pups were placed with C57 dams, and C57 females served as the subjects in binary choice tests between paired male urine odours (C57 vs. BALB, C57 vs. adopted BALB, and BALB vs. adopted BALB). In both experiments, we found that females preferred the urine of males from different genetic backgrounds, suggesting that female olfactory preferences may be driven by genetic compatibility. Cross-fostering had subtle effects on female olfactory preferences. Although the females showed no preference between the urine odours of adopted and non-adopted males of the other strain, the BALB females preferred the urine odour of BALB males to that of adopted C57 males, whereas the C57 females showed no preference between the urine odour of C57 and adopted BALB males. Using gas chromatography-mass spectrometry (GC-MS) and stepwise discriminant analysis, we found that the ratios of volatile chemicals from urine and preputial gland secretions were altered in the fostered male mice; these changes may have resulted in the behavioural changes observed in the females. Overall, the results suggest that female mice prefer urine odours from males with different genetic backgrounds; this preference may be driven by genetic compatibility. The early maternal environment influences the chemosignals of males and thus may influence the olfactory preferences of females. Our study provides additional evidence in support of genotype-dependent maternal influences on phenotypic variability in adulthood.

Project description:Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

Dataset Information

Sensory detection of female olfactory cues as a central regulator of energy metabolism and body weight in male mice.

Publications

Sensory detection of female olfactory cues as a central regulator of energy metabolism and body weight in male mice.

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